Modeling HSV-1 latency in human embryonic stem cell-derived neurons

Pathogens

Volumn 6, Issue 2, 2017, Pages

  Pourchet, Aldo ^a   Modrek, Aram S ^a   Placantonakis, Dimitris G ^a   Mohr, Ian ^a   Wilson, Angus C ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Alphaherpesvirus; Embryonic stem cells; Herpes simplex virus; HSV 1; Human; Latency; Primary neurons; Reactivation

Indexed keywords

ACICLOVIR; ALPHA INTERFERON; BUTYRIC ACID;

ANTIVIRAL THERAPY; ARTICLE; CELL DIFFERENTIATION; DISEASE MODEL; GENE EXPRESSION; HERPES SIMPLEX; HERPES SIMPLEX VIRUS 1; HUMAN; HUMAN CELL; HUMAN EMBRYONIC STEM CELL; IMMUNOFLUORESCENCE; NERVE CELL CULTURE; NONHUMAN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; RNA TRANSCRIPTION; VIRUS LATENCY; VIRUS LOAD; VIRUS REACTIVATION; VIRUS REPLICATION;

EID: 85020918547     PISSN: None     EISSN: 20760817     Source Type: Journal    
DOI: 10.3390/pathogens6020024     Document Type: Article

References (79)

1. Knipe, D.M., Howley, P.M. Fields Virology, 6th ed., LippincottWilliams & Wilkins: Philadelphia, PA, USA, 2013, Volume 1+2, pp. 1-2664.
2. Nagel, M.A., Choe, A., Traktinskiy, I., Gilden, D.H. Burning mouth syndrome due to herpes simplex virus type 1. BMJ Case Rep. 2015, 2015, bcr2015209488.
3. Gilden, D.H., Mahalingam, R., Cohrs, R.J., Tyler, K.L. Herpesvirus infections of the nervous system. Nat. Clin. Pract. Neurol. 2007, 3, 82-94.
4. Wagner, E.K., Bloom, D.C. Experimental investigation of herpes simplex virus latency. Clin. Microbiol. Rev. 1997, 10, 419-443.
5. Wilson, A.C., Mohr, I. A cultured affair: HSV latency and reactivation in neurons. Trends Microbiol. 2012, 20, 604-611.
6. Webre, J.M., Hill, J.M., Nolan, N.M., Clement, C., McFerrin, H.E., Bhattacharjee, P.S., Hsia, V., Neumann, D.M., Foster, T.P., Lukiw, W.J., et al. Rabbit and mouse models of HSV-1 latency, reactivation, and recurrent eye diseases. J. Biomed. Biotechnol. 2012, 2012, 612316.
7. Laibson, P.R., Kibrick, S. Recurrence of herpes simplex virus in rabbit eyes: Results of a three-year study. Investig. Ophthalmol. 1969, 8, 346-350.
8. Hill, J.M., Dudley, J.B., Shimomura, Y., Kaufman, H.E. Quantitation and kinetics of induced HSV-1 ocular shedding. Curr. Eye Res. 1986, 5, 241-246.
9. Speck, P.G., Simmons, A. Divergent molecular pathways of productive and latent infection with a virulent strain of herpes simplex virus type 1. J. Virol. 1991, 65, 4001-4005.
10. Deatly, A.M., Spivack, J.G., Lavi, E., O’Boyle, D.R., Fraser, N.W. Latent herpes simplex virus type 1 transcripts in peripheral and central nervous system tissues of mice map to similar regions of the viral genome. J. Virol. 1988, 62, 749-756.
11. Spivack, J.G., Fraser, N.W. Detection of herpes simplex virus type 1 transcripts during latent infection in mice. J. Virol. 1987, 61, 3841-3847.
12. Devi-Rao, G.B., Bloom, D.C., Stevens, J.G., Wagner, E.K. Herpes simplex virus type 1 DNA replication and gene expression during explant-induced reactivation of latently infected murine sensory ganglia. J. Virol. 1994, 68, 1271-1282.
13. Knotts, F.B., Cook, M.L., Stevens, J.G. Pathogenesis of herpetic encephalitis in mice after ophthalmic inoculation. J. Infect. Dis. 1974, 130, 16-27.
14. Leib, D.A., Coen, D.M., Bogard, C.L., Hicks, K.A., Yager, D.R., Knipe, D.M., Tyler, K.L., Schaffer, P.A. Immediate-early regulatory gene mutants define different stages in the establishment and reactivation of herpes simplex virus latency. J. Virol. 1989, 63, 759-768.
15. Sawtell, N.M., Thompson, R.L. Rapid in vivo reactivation of herpes simplex virus in latently infected murine ganglionic neurons after transient hyperthermia. J. Virol. 1992, 66, 2150-2156.
16. Laycock, K.A., Lee, S.F., Brady, R.H., Pepose, J.S. Characterization of a murine model of recurrent herpes simplex viral keratitis induced by ultraviolet B radiation. Investig. Ophthalmol. Vis. Sci. 1991, 32, 2741-2746.
17. Steiner, I., Mador, N., Reibstein, I., Spivack, J.G., Fraser, N.W. Herpes simplex virus type 1 gene expression and reactivation of latent infection in the central nervous system. Neuropathol. Appl. Neurobiol. 1994, 20, 253-260.
18. Verweij, M.C., Ressing, M.E., Knetsch, W., Quinten, E., Halenius, A., van Bel, N., Hengel, H., Drijfhout, J.W., van Hall, T., Wiertz, E.J.H.J. Inhibition of mouse TAP by immune evasion molecules encoded by non-murine herpesviruses. Mol. Immunol. 2011, 48, 835-845.
19. Kim, J.Y., Mandarino, A., Chao, M.V., Mohr, I., Wilson, A.C. Transient Reversal of Episome Silencing Precedes VP16-Dependent Transcription during Reactivation of Latent HSV-1 in Neurons. PLoS Pathog. 2012, 8, e1002540.
20. Cleary, M.A., Stern, S., Tanaka, M., Herr, W. Differential positive control by Oct-1 and Oct-2: Activation of a transcriptionally silent motif through Oct-1 and VP16 corecruitment. Genes Dev. 1993, 7, 72-83.
21. Camarena, V., Kobayashi, M., Kim, J.Y., Roehm, P.C., Perez, R., Gardner, J., Wilson, A.C., Mohr, I., Chao, M.V. Nature and duration of growth factor signaling through receptor tyrosine kinases regulates HSV-1 latency in neurons. Cell Host Microbe 2010, 8, 320-330.
22. Kobayashi, M., Wilson, A.C., Chao, M.V., Mohr, I. Control of viral latency in neurons by axonal mTOR signaling and the 4E-BP translation repressor. Genes Dev. 2012, 26, 1527-1532.
23. Cliffe, A.R., Arbuckle, J.H., Vogel, J.L., Geden, M.J., Rothbart, S.B., Cusack, C.L., Strahl, B.D., Kristie, T.M., Deshmukh, M. Neuronal Stress Pathway Mediating a Histone Methyl/Phospho Switch Is Required for Herpes Simplex Virus Reactivation. Cell Host Microbe 2015, 18, 649-658.
24. Jurak, I., Hackenberg, M., Kim, J.Y., Pesola, J.M., Everett, R.D., Preston, C.M., Wilson, A.C., Coen, D.M. Expression of Herpes Simplex Virus 1 miRNAs in Cell Culture Models of Quiescent and Latent Infection. J. Virol. 2014, 88, 2337-2339.
25. Linderman, J.A., Kobayashi, M., Rayannavar, V., Fak, J.J., Darnell, R.B., Chao, M.V., Wilson, A.C., Mohr, I. Immune Escape via a Transient Gene Expression Program Enables Productive Replication of a Latent Pathogen. Cell Rep. 2017, 18, 1312-1323.
26. Kim, J.Y., Shiflett, L.A., Linderman, J.A., Mohr, I., Wilson, A.C. Using homogeneous primary neuron cultures to study fundamental aspects of HSV-1 latency and reactivation. Methods Mol. Biol. 2014, 1144, 167-179.
27. Kobayashi, M., Kim, J.Y., Camarena, V., Roehm, P.C., Chao, M.V., Wilson, A.C., Mohr, I. A primary neuron culture system for the study of herpes simplex virus latency and reactivation. J. Vis. Exp. 2012, 62, e3823.
28. Wilcox, C.L., Smith, R.L., Freed, C.R., Johnson, E.M. Nerve growth factor-dependence of herpes simplex virus latency in peripheral sympathetic and sensory neurons in vitro. J. Neurosci. 1990, 10, 1268-1275.
29. Wilcox, C.L., Johnson, E.M. Characterization of nerve growth factor-dependent herpes simplex virus latency in neurons in vitro. J. Virol. 1988, 62, 393-399.
30. Wilcox, C.L., Johnson, E.M. Nerve growth factor deprivation results in the reactivation of latent herpes simplex virus in vitro. J. Virol. 1987, 61, 2311-2315.
31. Roehm, P.C., Camarena, V., Nayak, S., Gardner, J.B., Wilson, A., Mohr, I., Chao, M.V. Cultured vestibular ganglion neurons demonstrate latent HSV1 reactivation. Laryngoscope 2011, 121, 2268-2275.
32. Kuhn, M.A., Nayak, S., Camarena, V., Gardner, J., Wilson, A., Mohr, I., Chao, M.V., Roehm, P.C. A cell culture model of facial palsy resulting from reactivation of latent herpes simplex type 1. Otol. Neurotol. 2012, 33, 87-92.
33. Avgousti, D.C., Weitzman, M.D. Stress Flips a Chromatin Switch to Wake Up Latent Virus. Cell Host Microbe 2015, 18, 639-641.
34. Cliffe, A.R., Wilson, A.C. Restarting Lytic Gene Transcription at the Onset of Herpes Simplex Virus Reactivation. J. Virol. 2017, 91, e01419-16.
35. Azarkh, Y., Bos, N., Gilden, D.H., Cohrs, R.J. Human trigeminal ganglionic explants as a model to study alphaherpesvirus reactivation. J. Neurovirol. 2012, 18, 456-461.
36. Cohrs, R.J., Laguardia, J.J., Gilden, D.H. Distribution of latent herpes simplex virus type-1 and varicella zoster virus DNA in human trigeminal Ganglia. Virus Genes 2005, 31, 223-227.
37. Cohrs, R.J., Randall, J., Smith, J., Gilden, D.H., Dabrowski, C., van Der Keyl, H., Tal-Singer, R. Analysis of individual human trigeminal ganglia for latent herpes simplex virus type 1 and varicella-zoster virus nucleic acids using real-time PCR. J. Virol. 2000, 74, 11464-11471.
38. Yu, X., Seitz, S., Pointon, T., Bowlin, J.L., Cohrs, R.J., Jonjic, S., Haas, J., Wellish, M., Gilden, D.H. Varicella zoster virus infection of highly pure terminally differentiated human neurons. J. Neurovirol. 2013, 19, 75-81.
39. Pugazhenthi, S., Nair, S., Velmurugan, K., Liang, Q., Mahalingam, R., Cohrs, R.J., Nagel, M.A., Gilden, D.H. Varicella-zoster virus infection of differentiated human neural stem cells. J. Virol. 2011, 85, 6678-6686.
40. Lee, K.S., Zhou, W., Scott-McKean, J.J., Emmerling, K.L., Cai, G.-Y., Krah, D.L., Costa, A.C., Freed, C.R., Levin, M.J. Human sensory neurons derived from induced pluripotent stem cells support varicella-zoster virus infection. PLoS ONE 2012, 7, e53010.
41. Markus, A., Grigoryan, S., Sloutskin, A., Yee, M.B., Zhu, H., Yang, I.H., Thakor, N.V., Sarid, R., Kinchington, P.R., Goldstein, R.S. Varicella-zoster virus (VZV) infection of neurons derived from human embryonic stem cells: Direct demonstration of axonal infection, transport of VZV, and productive neuronal infection. J. Virol. 2011, 85, 6220-6233.
42. Sadaoka, T., Depledge, D.P., Rajbhandari, L., Venkatesan, A., Breuer, J., Cohen, J.I. In vitro system using human neurons demonstrates that varicella-zoster vaccine virus is impaired for reactivation, but not latency. Proc. Natl. Acad. Sci. USA 2016, 113, E2403-E2412.
43. Thomson, J.A., Itskovitz-Eldor, J., Shapiro, S.S., Waknitz, M.A., Swiergiel, J.J., Marshall, V.S., Jones, J.M. Embryonic stem cell lines derived from human blastocysts. Science 1998, 282, 1145-1147.
44. Tabar, V., Panagiotakos, G., Greenberg, E.D., Chan, B.K., Sadelain, M., Gutin, P.H., Studer, L. Migration and differentiation of neural precursors derived from human embryonic stem cells in the rat brain. Nat. Biotechnol. 2005, 23, 601-606.
45. Placantonakis, D.G., Tomishima, M.J., Lafaille, F., Desbordes, S.C., Jia, F., Socci, N.D., Viale, A., Lee, H., Harrison, N., Tabar, V., et al. BAC transgenesis in human embryonic stem cells as a novel tool to define the human neural lineage. Stem Cells 2009, 27, 521-532.
46. Edri, R., Yaffe, Y., Ziller, M.J., Mutukula, N., Volkman, R., David, E., Jacob-Hirsch, J., Malcov, H., Levy, C., Rechavi, G., et al. Analysing human neural stem cell ontogeny by consecutive isolation of Notch active neural progenitors. Nat. Commun. 2015, 6, 6500.
47. Lendahl, U., Zimmerman, L.B., McKay, R.D. CNS stem cells express a new class of intermediate filament protein. Cell 1990, 60, 585-595.
48. Dahlstrand, J., Lardelli, M., Lendahl, U. Nestin mRNA expression correlates with the central nervous system progenitor cell state in many, but not all, regions of developing central nervous system. Brain Res. Dev. Brain Res. 1995, 84, 109-129.
49. D’Aiuto, L., Zhi, Y., Kumar Das, D., Wilcox, M.R., Johnson, J.W., McClain, L., MacDonald, M.L., Di Maio, R., Schurdak, M.E., Piazza, P., et al. Large-scale generation of human iPSC-derived neural stem cells/early neural progenitor cells and their neuronal differentiation. Organogenesis 2014, 10, 365-377.
50. Brown, J.P., Couillard-Després, S., Cooper-Kuhn, C.M., Winkler, J., Aigner, L., Kuhn, H.G. Transient expression of doublecortin during adult neurogenesis. J. Comp. Neurol. 2003, 467, 1-10.
51. Walker, T.L., Yasuda, T., Adams, D.J., Bartlett, P.F. The doublecortin-expressing population in the developing and adult brain contains multipotential precursors in addition to neuronal-lineage cells. J. Neurosci. 2007, 27, 3734-3742.
52. Benboudjema, L., Mulvey, M., Gao, Y., Pimplikar, S.W., Mohr, I. Association of the herpes simplex virus type 1 Us11 gene product with the cellular kinesin light-chain-related protein PAT1 results in the redistribution of both polypeptides. J. Virol. 2003, 77, 9192-9203.
53. Phelan, D., Barrozo, E.R., Bloom, D.C. HSV1 latent transcription and non-coding RNA: A critical retrospective. J. Neuroimmunol. 2017.
54. Galloway, D.A., Fenoglio, C., Shevchuk, M., McDougall, J.K. Detection of herpes simplex RNA in human sensory ganglia. Virology 1979, 95, 265-268.
55. Hafezi, W., Lorentzen, E.U., Eing, B.R., Müller, M., King, N.J. C., Klupp, B., Mettenleiter, T.C., Kühn, J.E. Entry of Herpes Simplex Virus Type 1 (HSV-1) into the Distal Axons of Trigeminal Neurons Favors the Onset of Nonproductive, Silent Infection. PLoS Pathog. 2012, 8, e1002679.
56. Daigle, D., Gradoville, L., Tuck, D., Schulz, V., Wang’ondu, R., Ye, J., Gorres, K., Miller, G. Valproic acid antagonizes the capacity of other histone deacetylase inhibitors to activate the Epstein-barr virus lytic cycle. J. Virol. 2011, 85, 5628-5643.
57. Luka, J., Kallin, B., Klein, G. Induction of the Epstein-Barr virus (EBV) cycle in latently infected cells by n-butyrate. Virology 1979, 94, 228-231.
58. Ertel, M.K., Cammarata, A.L., Hron, R.J., Neumann, D.M. CTCF occupation of the HSV-1 genome is disrupted at early times post-reactivation in a transcription-dependent manner. J. Virol. 2012, 86, 12741-12759.
59. Danaher, R.J., Jacob, R.J., Steiner, M.R., Allen, W.R., Hill, J.M., Miller, C.S. Histone deacetylase inhibitors induce reactivation of herpes simplex virus type 1 in a latency-associated transcript-independent manner in neuronal cells. J. Neurovirol. 2005, 11, 306-317.
60. Neumann, D.M., Bhattacharjee, P.S., Hill, J.M. Sodium butyrate: A chemical inducer of in vivo reactivation of herpes simplex virus type 1 in the ocular mouse model. J. Virol. 2007, 81, 6106-6110.
61. Yanez, A., Harrell, T., Sriranganathan, H., Ives, A., Bertke, A. Neurotrophic Factors NGF, GDNF and NTN Selectively Modulate HSV1 and HSV2 Lytic Infection and Reactivation in Primary Adult Sensory and Autonomic Neurons. Pathogens 2017, 6, 5.
62. Enquist, L.W., Leib, D.A. Intrinsic and innate defenses of neurons: Détente with the herpesviruses. J. Virol. 2016, 91.
63. Leib, D.A., Harrison, T.E., Laslo, K.M., Machalek, M.A., Moorman, N.J., Virgin, H.W. Interferons regulate the phenotype of wild-type and mutant herpes simplex viruses in vivo. J. Exp. Med. 1999, 189, 663-672.
64. Luker, G.D., Prior, J.L., Song, J., Pica, C.M., Leib, D.A. Bioluminescence imaging reveals systemic dissemination of herpes simplex virus type 1 in the absence of interferon receptors. J. Virol. 2003, 77, 11082-11093.
65. Rosato, P.C., Leib, D.A. Neuronal Interferon Signaling Is Required for Protection against Herpes Simplex Virus Replication and Pathogenesis. PLoS Pathog. 2015, 11, e1005028.
66. Bloom, D.C. Alphaherpesvirus Latency: A Dynamic State of Transcription and Reactivation. Adv. Virus Res. 2016, 94, 53-80.
67. Orzalli, M.H., Conwell, S.E., Berrios, C., DeCaprio, J.A., Knipe, D.M. Nuclear interferon-inducible protein 16 promotes silencing of herpesviral and transfected DNA. Proc. Natl. Acad. Sci. USA 2013, 110, E4492-E4501.
68. Lo, C.I., De Andrea, M., Borgogna, C., Albertini, S., Landini, M.M., Peretti, A., Johnson, K.E., Chandran, B., Landolfo, S., Gariglio, M. TheNuclearDNASensor IFI16Acts as a Restriction Factor forHuman Papillomavirus Replication through Epigenetic Modifications of the Viral Promoters. J. Virol. 2015, 89, 7506-7520.
69. Johnson, K.E., Bottero, V., Flaherty, S., Dutta, S., Singh, V.V., Chandran, B. IFI16 Restricts HSV-1 Replication by Accumulating on the HSV-1 Genome, Repressing HSV-1 Gene Expression, and Directly or Indirectly Modulating Histone Modifications. PLoS Pathog. 2014, 10, e1004503.
70. Szpara, M.L., Kobiler, O., Enquist, L.W. A common neuronal response to alphaherpesvirus infection. J. Neuroimmune Pharmacol. 2010, 5, 418-427.
71. Bertke, A.S., Swanson, S.M., Chen, J., Imai, Y., Kinchington, P.R., Margolis, T.P. A5-positive primary sensory neurons are nonpermissive for productive infection with herpes simplex virus 1 in vitro. J. Virol. 2011, 85, 6669-6677.
72. Warren, K.G., Brown, S.M., Wroblewska, Z., Gilden, D.H., Koprowski, H., Subak-Sharpe, J. Isolation of latent herpes simplex virus from the superior cervical and vagus ganglions of human beings. N. Engl. J. Med. 1978, 298, 1068-1069.
73. Lafferty, W.E., Coombs, R.W., Benedetti, J., Critchlow, C., Corey, L. Recurrences after oral and genital herpes simplex virus infection. Influence of site of infection and viral type. N. Engl. J. Med. 1987, 316, 1444-1449.
74. Mertens, J., Marchetto, M.C., Bardy, C., Gage, F.H. Evaluating cell reprogramming, differentiation and conversion technologies in neuroscience. Nat. Rev. Neurosci. 2016, 17, 424-437.
75. Blanchard, J.W., Eade, K.T., Szucs, A., Lo Sardo, V., Tsunemoto, R.K., Williams, D., Sanna, P.P., Baldwin, K.K. Selective conversion of fibroblasts into peripheral sensory neurons. Nat. Neurosci. 2015, 18, 25-35.
76. Markus, A., Lebenthal-Loinger, I., Yang, I.H., Kinchington, P.R., Goldstein, R.S. An in vitro model of latency and reactivation of varicella zoster virus in human stem cell-derived neurons. PLoS Pathog. 2015, 11, e1004885.
77. Christensen, J., Steain, M., Slobedman, B., Abendroth, A. Differentiated neuroblastoma cells provide a highly efficient model for studies of productive varicella-zoster virus infection of neuronal cells. J. Virol. 2011, 85, 8436-8442.
78. Sun, Z., Yang, H., Shi, Y., Wei, M., Xian, J., Hu, W. [Establishment of a cell model system of herpes simplex virus type II latent infection and reactivation in SH-SY5Y cells]. Wei Sheng Wu Xue Bao 2010, 50, 98-106.
79. Thellman, N.M., Botting, C., Madaj, Z., Triezenberg, S.J. An Immortalized Human Dorsal Root Ganglia Cell Line Provides a Novel Context to Study Herpes Simplex Virus Type-1 Latency and Reactivation. J. Virol. 2017, 91.